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. 2017 Jun 8;12(6):e0178324.
doi: 10.1371/journal.pone.0178324. eCollection 2017.

Association of vaginal dysbiosis and biofilm with contraceptive vaginal ring biomass in African women

Liselotte Hardy  1   2 , Vicky Jespers  1 , Irith De Baetselier  2 , Jozefien Buyze  3 , Lambert Mwambarangwe  4 , Viateur Musengamana  4 , Janneke van de Wijgert  4   5 , Tania Crucitti  2
Affiliations

Association of vaginal dysbiosis and biofilm with contraceptive vaginal ring biomass in African women

Liselotte Hardy et al. PLoS One. .

Abstract

We investigated the presence, density and bacterial composition of contraceptive vaginal ring biomass and its association with the vaginal microbiome. Of 415 rings worn by 120 Rwandese women for three weeks, the biomass density was assessed with crystal violet and the bacterial composition of biomass eluates was assessed with quantitative polymerase chain reaction (qPCR). The biomass was visualised after fluorescence in situ hybridisation (FISH) and with scanning electron microscopy (SEM). The vaginal microbiome was assessed with Nugent scoring and vaginal biofilm was visualised after FISH. All vaginal rings were covered with biomass (mean optical density (OD) of 3.36; standard deviation (SD) 0.64). Lactobacilli were present on 93% of the rings, Gardnerella vaginalis on 57%, and Atopobium vaginae on 37%. The ring biomass density was associated with the concentration of A. vaginae (OD +0.03; 95% confidence interval (CI) 0.01-0.05 for one log increase; p = 0.002) and of G. vaginalis (OD +0.03; (95% CI 0.01-0.05; p = 0.013). The density also correlated with Nugent score: rings worn by women with a BV Nugent score (mean OD +0.26), and intermediate score (mean OD +0.09) had a denser biomass compared to rings worn by participants with a normal score (p = 0.002). Furthermore, presence of vaginal biofilm containing G. vaginalis (p = 0.001) and A. vaginae (p = 0.005) correlated with a denser ring biomass (mean OD +0.24 and +0.22 respectively). With SEM we observed either a loose network of elongated bacteria or a dense biofilm. We found a correlation between vaginal dysbiosis and the density and composition of the ring biomass, and further research is needed to determine if these relationships are causal. As multipurpose vaginal rings to prevent pregnancy, HIV, and other sexually transmitted diseases are being developed, the potential impact of ring biomass on the vaginal microbiota and the release of active pharmaceutical ingredients should be researched in depth.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1
Visualisation of biomass on intravaginal ring surface by confocal laser scanning microscopy after fluorescence in situ hybridisation at 400x magnification: A. Lactobacilli (Lactobacillus spp. PNA-probe Lac663 with Alex Fluor 647 in red) scattered on vaginal epithelial cells (DNA stain with 4’,6-diamidino-2-phenylindole (DAPI) in blue); B. Vaginal epithelial cells DNA stain with DAPI in blue) partially covered with bacterial biofilm (G. vaginalis specific PNA-probe Gard162 with Alexa Fluor 647 in red and A. vaginae specific PNA-probe AtoITM1 with Alexa Fluor 488 in green).
Fig 2
Fig 2. Visualisation of biomass on intravaginal ring surface by scanning electron microscopy at 23x magnification.
Fig 3
Fig 3
Visualisation of biomass on intravaginal ring surface by scanning electron microscopy at A. 1000x and B. 4000x magnification: Phenotype 1—elongated bacteria scattered on vaginal epithelial cells.
Fig 4
Fig 4
Visualisation of biomass on intravaginal ring surface by scanning electron microscopy at A. 1000x and B. 4000x magnification: Phenotype 2—condense biofilm of bacilli on vaginal epithelial cells.
See this image and copyright information in PMC

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